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Evidence for Character Displacement in Floral Scent

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Evidence for Character Displacement in Floral Scent bioRxiv preprint doi: https://doi.org/10.1101/2020.04.02.022004; this version posted April 3, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Emission rates of species-specific volatiles change across communities of Clarkia species: 2 Evidence for character displacement in floral scent. 3 Katherine E. Eisen1,2, Monica A. Geber1, Robert A. Raguso3 4 1 Department of Ecology and Evolutionary Biology, Cornell University, Ithaca NY, 5 14853, USA. 6 2 Email for correspondence: [email protected] 7 3 Department of Neurobiology and Behavior, Cornell University, Ithaca NY, 14853, 8 USA. 9 Keywords: allopatry, sympatry, multimodal floral traits, context-dependent selection 10 Word count: 5,864 words 11 This manuscript contains four figures and one table in the main text, two methodological 12 appendices, and six supplemental tables. 13 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.02.022004; this version posted April 3, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 14 Abstract 15 A current frontier of character displacement research is to determine if displacement occurs via 16 multiple phenotypic pathways and varies across communities with different species 17 compositions. Here, we conducted the first test for context-dependent character displacement in 18 multimodal floral signals by analyzing variation in floral scent in a system that exhibits character 19 displacement in flower size, and that has multiple types of sympatric communities. In a 20 greenhouse common garden experiment, we measured quantitative variation in volatile emission 21 rates of the progeny of two species of Clarkia from replicated communities that contain one, 22 two, or four Clarkia species. The first two axes of a constrained correspondence analysis, which 23 explained 24 percent of the total variation in floral scent, separated the species and community 24 types, respectively. Of the 23 compounds that were significantly correlated with these axes, nine 25 showed patterns consistent with character displacement. Two compounds produced primarily by 26 C. unguiculata and two compounds produced primarily by C. cylindrica were emitted in higher 27 amounts in sympatry. Character displacement in some volatiles varied across sympatric 28 communities and occurred in parallel with displacement in flower size, demonstrating that this 29 evolutionary process can be context-dependent and may occur through multiple pathways. bioRxiv preprint doi: https://doi.org/10.1101/2020.04.02.022004; this version posted April 3, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 30 31 Introduction 32 Interspecific interactions have long been hypothesized to have significant effects on 33 patterns of biodiversity (Darwin 1859; Lack 1945; Schluter 2000; Grant and Grant 2008). One 34 such evolutionary process is character displacement, which leads to a pattern of differences in 35 species’ trait values in sympatric communities relative to allopatric communities (Brown and 36 Wilson 1956; Germain et al. 2017). While character displacement has been studied and debated 37 for over sixty years (Stuart and Losos 2013), there are two key gaps in our understanding of this 38 process. First, outside of a small number of classic systems (e.g., anoles, sticklebacks, Darwin’s 39 finches), few studies have examined the potential for character displacement in more than one 40 type of trait (reviewed in Stuart and Losos 2013). Examining variation in multiple types of traits 41 increases our ability to detect non-repeatable character displacement, which may occur through 42 different phenotypic pathways across communities (Losos 2011; Germain et al. 2017), and 43 determine when species interactions lead to shifts in correlated or independently-evolving traits. 44 Second, while most studies of character displacement have focused on pairwise interactions (but 45 see Lemmon and Lemmon 2010; Miller et al. 2014a; Grant 2017; Roth-Monzon et al. 2020), 46 many species exist in complex ecological communities, where interactions with multiple species 47 could include indirect and higher-order interactions (Mayfield and Stouffer 2017; TerHorst et al. 48 2018; Roth-Monzon et al. 2020). Testing for character displacement across sympatric 49 communities that vary in species composition or richness (Eisen and Geber 2018; Roth-Monzon 50 et al. 2020) can advance our understanding of the evolutionary consequences of direct and 51 indirect interactions (Walsh 2013; TerHorst et al. 2015). bioRxiv preprint doi: https://doi.org/10.1101/2020.04.02.022004; this version posted April 3, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 52 Among co-occurring flowering plants, pollinators often represent a shared resource that is 53 critical for reproduction (Waser et al. 1996; Ollerton et al. 2011), and there is a growing body of 54 evidence for character displacement in plants mediated by interactions between co-occurring 55 species that share pollinators (reviewed in Beans 2014; Eisen and Geber 2018). Presently, there 56 are two critical gaps in our understanding of this process. First, studies to date have examined 57 character displacement in floral morphology, color, and phenology (reviewed in Beans 2014; 58 Eisen and Geber 2018), which reflects a general bias towards visual traits in pollination (Raguso 59 2008a). Nonetheless, olfactory and reward traits are critical to successful pollination in many 60 systems (Schiestl 2010, 2015; Raguso 2014) but have yet to be integrated in to the study of 61 character displacement. Second, character displacement in floral traits is likely to occur via 62 multiple phenotypic pathways or changes in trait combinations across communities (Losos 2011; 63 Germain et al. 2017). Nonetheless, most studies to date have addressed character displacement in 64 one type of floral trait (e.g., color or morphology), not the multi-modal bouquet flowers typically 65 present (Leonard et al. 2011). 66 The emission of floral scent—volatile organic compounds including monoterpenes, 67 sesquiterpenes, and aromatic compounds (Knudsen et al. 2006)—is a complex trait, in that 68 individual plants can exhibit qualitative variation in the blend of volatiles and quantitative 69 variation in their emission rates (Raguso 2008b). Because scent can be produced not only from 70 petals but also from reproductive floral structures, scent may be correlated with or unrelated to 71 variation in flower size (Effmert et al. 2006; Valdivia and Niemeyer 2006; Burdon et al. 2015; 72 Martin et al. 2017), which could lead to multi-modal character displacement in some systems. In 73 addition, species may vary in common volatiles that are produced by a small number of 74 biosynthetic pathways (Dudareva and Pichersky 2006), and in species-specific volatiles that bioRxiv preprint doi: https://doi.org/10.1101/2020.04.02.022004; this version posted April 3, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 75 provide ‘private channels’ for communication with specialist pollinators (Raguso 2008b; Soler et 76 al. 2010). Insights from three areas of floral scent research suggest that floral scent could 77 undergo character displacement. First, floral scent exhibits substantial intraspecific variation 78 across populations in multiple systems, including cacti (Schlumpberger and Raguso 2008), 79 cycads (Suinyuy et al. 2012), saxifrages (Friberg et al. 2019), and orchids (Gross et al. 2016; 80 Chapurlat et al. 2018). These patterns suggest that floral scent may be relatively evolutionarily 81 labile. As a result, scent could evolve in response to geographic variation in selection (Gross et 82 al. 2016), which could lead to variation in character displacement across different communities 83 (Germain et al. 2017; Eisen and Geber 2018). Second, floral scent can be a target of pollinator- 84 mediated selection (Parachnowitsch et al. 2012; Chapurlat et al. 2019), which indicates that floral 85 scent could evolve in response to interactions between co-occurring plant species that share 86 pollinators. Third, differences in floral scent can mediate reproductive isolation between co- 87 occurring species (Waelti et al. 2008; Bischoff et al. 2014; Peakall and Whitehead 2014) and 88 explain variation in the structure of plant-pollinator networks (Junker et al. 2010; Larue et al. 89 2016; Kantsa et al. 2018, 2019). As such, floral scent may determine how pollinators are 90 partitioned among co-occurring plant species. 91 In this study, we test for variation in multimodal character displacement across sympatric 92 communities that contain different numbers of co-occurring species. Specifically, we assess the 93 potential for character displacement in the floral scent of two co-occurring species of California 94 native annuals in the genus Clarkia (Onagraceae). These species, C. unguiculata and C. 95 cylindrica, co-occur more frequently than expected by chance in the southern foothills of the 96 Sierra Nevada (Kern County, CA, USA). Where they co-occur, these species have converged in 97 flowering time and diverged in flower size (Eisen and Geber 2018). This pattern of divergence in bioRxiv preprint doi: https://doi.org/10.1101/2020.04.02.022004; this version posted April 3, 2020.
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